Epigenetic regulation and memory of convergent temperature–light signaling: Insights from Arabidopsis and implications for crop phenotypic plasticity

Abstract

Plants simultaneously experience temperature and light, yet whether these cues interact at the chromatin level to generate distinct regulatory states remains unresolved. This review establishes a hierarchical evidence framework, ranging from single-factor responsiveness to causal functional validation, to critically evaluate claims of photothermal epigenetic integration. We synthesize evidence across major regulatory modules (phyB–PIF, COP1–SPA, ELF3) and chromatin mechanisms (H2A.Z dynamics, histone modifications, DNA methylation). Our analysis reveals substantial convergence of temperature and light at signaling and transcriptional nodes, and robust evidence that each cue independently influences chromatin. However, direct evidence for a non-additive temperature × light chromatin state with demonstrated causal function is scarce, primarily due to the rarity of factorial experiments that can distinguish interaction effects from additive responses. The rice ACT1 study exemplifies rigorous causal epigenetic validation but investigates cold stress alone, highlighting the need for photothermal factorial designs. We extend this framework to crop improvement and vegetatively propagated species such as enset, where clonal reproduction offers opportunities to investigate epigenetic persistence. Crucially, we emphasize that persistence alone cannot establish adaptive inheritance—stability, phenotypic effects, transmission, and fitness consequences require independent evaluation. Resolving when combined temperature and light produce functionally consequential chromatin states will determine whether photothermal epigenetic regulation represents a bona fide mechanism of environmental plasticity or primarily a correlate of broader physiological responses. Although plants clearly exhibit heat-stress memory and integrate temperature and light through interconnected signaling and chromatin-regulatory networks, there is still limited direct evidence that combined heat and light exposure generates a distinct, integrated epigenetic memory that cannot be explained by the individual or interacting effects of each cue. More controlled factorial experiments are needed to determine whether combined temperature–light histories produce unique and persistent molecular states. This review provides a rigorous interpretive lens for evaluating evidence and identifies priority experimental approaches needed to establish or refute photothermal epigenetic integration.